Epicardial surface dynamics in the closed-chest normal canine

Pergamon

J. Biomechmics,

0021-9290(95)oooO4-6

EPICARDIAL

Vol. 28, No. 11, pp. 1319-1332, 1995 Copy@& 0 1995 Elsevier Science Ltd Printed in Great Britain. All rights merved 0021-92w95 $9.50 + .oo

SURFACE DYNAMICS IN THE CLOSED-CHEST NORMAL CANINE

JosephJ. McInerney, Emily F. Kim, Michael D. Herr and Gary L. Copenhaver ThePennsylvania StateUniversity,Department of Medicine and Bioengineering, The Milton S. Hershey Medical Center, Hershey, PA 17033, U.S.A.

Abstract-Past studies of the changing three-dimensional shape of the heart in the closed chest during the cardiac cycle have been restricted to the measurement of local deformations at a relatively few specific locations, and often have required surgical procedures that alter the measurements obtained. In the study reported here, high precision displacement and velocity measurements were obtained at the epicardial interface using a Compton backscatter imaging technique that does not require a surgical intervention or contrast injections. Displacement and velocity measurements were obtained at more than 200 locations at the epicardial interface at 13 ms intervals throughout the cardiac cycle. Measurements of the changing shape of the heart during the cardiac cycle with this technique are precise to 0.1 mm (S.D.). Displacement and velocity patterns recorded in this study confirm and integrate the studies of many others and also add new information. An unexpected vigorous inward motion of both the LV (39 mrns- ‘) and RV (26 mms-i) surfaces during isovolumic relaxation and early rapid retill is demonstrated. Velocities during this period equal or exceed those that occur during ejection. During ejection, inward LV motion at the base of the heart precedes that at the apex by 8&90 ms. Posterior LV displacements and velocities during ejection are 4-6 times greater than those at the anterior and apex. The Compton backscatter imaging technique for obtaining undisturbed measurements of cardiac dynamics in the closed chest has potential as a non-invasive clinical tool for serial studies of cardiac surface motion abnormalities. The data presented can also be used to set surface boundary conditions for biomechanical models of heart deformation. Keywords: Epicardiah Wall motion; Canines; Non-invasive; Heart.

angiography to evaluate cardiac pathology, angiographic data are quite limited in providing reliabledata Interest in the changing geometry of the normal heart for modelingstudies. during the cardiac cycle hascontinued from the classic Other techniqueshavetracked the motion patternsof observationsof the 17th century (Harvey, 1928)to the specific points on the myocardium using implanted presentday. This interesthasbeendriven by the needfor transducers,metallic markers,physiologicallandmarks a standard againstwhich to measurethe degreeof car- or MRI tagging techniques.Most of thesefixed marker diac pathology aswell asto provide basicmeasurements techniques,however, were usedin studiesrestricted to suitablefor the theoretical modelingof the heart. Many the measurement of globaldiameters,local deformations techniquesfor monitoring ventricular geometry have at only a few specificlocations,or the tracking of markers beendeveloped.The techniquemost frequently usedfor placedonly alonganterior and posteriorboundariescorstudying cardiac wall dynamicsis LV angiographyper- respondingto the 30” RAO projection used in most formedin a 30” right anterior oblique (RAO) projection. angiographicstudies.Many of thesemarker studiesalso This projection silhouettesthe mitral and aortic valve required surgical techniqueswhich themselveschange planes,the anterior and posterior boundariesof the LV the motion patternsbeingmeasured(Rankin et al., 1976). chamber,and presentsa long axis silhouetteof the ventThe goal of the work presentedin this paper is to ricle (Raphaeland Allwork, 1974).Angiography, how- provide a detailedstudy of the conformationalchangesof ever, yields little information on the three-dimensional the epicardial free walls of the heart throughout the shapeof the heart. Points contiguous on the cardiac cardiac cycle using a method that doesnot disturb the angiographicsilhouette neednot be contiguouson the heart in its natural environment. The study was persurfaceof the heart and the set of surfacepoints repres- formed with a high precisionnon-invasiveclosed-chest ented on the silhouetteedgechangesfrom moment to X-ray scatteringtechnique.This measurementtechnique moment. Although there has been some success in using doesnot require cutdowns,marker implantations,contrast injections,or other interventionsthat could disturb normal cardiacmotion patterns.The resultsof the study Received in final form 20 December 1994. confirm and integrate the findings of many others and Address correspondence to: Joseph J. McInemey, Ph.D., The add new information on normal cardiacdynamics.They Pennsylvania State University, The Milton S. Hershey Medical Center, Department of Medicine, Division of Cardiology, P.O. provide a basisfor constructing and testing theoretical modelsof the heart as well as for comparingdynamic Box 850, Hershey, PA 17033, U.S.A. IN’I’RODUCTION

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J. J. McInerney et al.

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cardiac shape changes that may be associated with pathology. The normal asymmetries in the shape of the heart during both ejection and early relaxation are clearly demonstrated, and their relation to events within the cardiac cycle are discussed. METHODS

Right and left ventricular epicardial free wall motion characteristics were studied in a series of 11 mongrel dogs of both sexes weighing between 18.6 and 25.9 kg. The protocol for these studies was approved by the Animal Care and Use Committee of the MS. Hershey Medical Center, The Pennsylvania State University, and according to the guidelines of the Committee on Care and Use of Laboratory Animals of the Institute of Laboratory Animal Resources, National Research Council. Each dog was initially anesthetized with an intravenous injection of pentothal. This was followed by an IV injection of a 6% solution of alpha-chloralose (1 cm3 kg- ‘) and subcutaneous morphine (15 mg kg- ‘). Maintenance doses of chloralose and morphine were given as needed. The dogs were placed in a supine position during all measurements and mechanically ventilated. Breath was held at endinspiration during data acquisition to eliminate respirat-

ory motion artifacts. A Millar microtip pressure transducer catheter was inserted via the femoral artery to measure left ventricular and aortic pressures. EKGs and left and right ventriculograms were recorded for each dog and hearts were paced at 90 bpm from the right atrium with a Grass S88G stimulator (Grass Instruments, Quincy, MA). Left and right free wall displacements and velocities were measured on each dog using a high precision Compton backscatter imaging (CBI) technique (McInerney et al., 1989). This technique in its elemental form is shown in Fig. 1. A ‘sensitive volume’, created by the intersection of the field of view of a collimated detector and a small diameter (-6 mm) X-ray beam, is rapidly scanned along the path of the X-ray beam to the heart. A simple pattern recognition algorithm is used to return the sensitive volume to the position where the detected Compton scatter signal is halfway between the lung minimum and myocardial maximum signals. At this position, the sensitive volume is approximately centered at the lung-epicardial interface and the time-varying amount of tissue filling the sensitive volume modulates the scatter signal output as the heart beats. The slope of the detector signal at the ‘half-max’ level between the lung minimum and myocardial maximum (Fig. 1) is linear and is used to convert the scatter signal output from

Fig. 1. CBI technique.Scatteredradiation is detectedwithin a sensitivevolume definedby the intersection of the field of view of a collimatedradiation detector and a narrow X-ray beam. When positioned at the epicardialinterface,displacementof the heart along the path of the X-ray beamwill modulate the detected radiation Scattersignal in proportion to the position of the epicardialinterfacewithin the sensitive volume. The absolute position of the interface at any instant is then determinedby combining the detector scan position with the relative location of the surface within the detector’s field of view.

Epicardial surface dynamics the detector into instantaneous surface displacements within the sensitive volume. The surface displacements within the sensitive volume are then related to an absolute external reference frame by adding the known scan position of the detector. With this technique, epicardial surface displacements, measured along the path of the X-ray beam, are digitized at 5 ms intervals with a ten-beat average precision of f 0.1 mm (S.D.) throughout the cardiac cycle (McInerney et al., 1984, 1989). Premature beats in these studies are rare and when they occur are not included in the ten-beat averages. For the studies reported here the displacements during the cardiac cycle were measured at ten horizontal locations (approximately 1 cm spacing) using a multidetector array and an X-ray fan beam at each of 12-14 vertical levels (5 mm spacing). A displacement mapping of the left and right ventricular surfaces using this technique requires approximately 1520 min for each surface. A two-dimensional cubic spline fit was next used to interpolate the displacement data in the horizontal and vertical directions to produce a uniform 4 mm x 4 mm displacement waveform grid. This procedure generally provided displacement data at approximately 150 grid locations at each of the left and right epicardial interfaces. Surface velocities at each data grid intersection were calculated from the displacement data using a three-point central difference algorithm. To facilitate data interpretation, surface animations were created by combining data grid coordinates (Fig. 2) with the respective displacement data (for example see Figs 3 and 4) acquired at each grid intersection at 25 time points during the cardiac cycle (McInerney et al., 1989). These animations are displayed on a Macintosh com-

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puter (Apple Computer, Inc., Cupertino, CA) at user selected speeds and with selected repetitive replays of segments of the cardiac cycle. Color coded velocity maps of the left and right ventricular surfaces (50 frames per cardiac cycle) were also created. Average left and right ventricular surfaces were created by combining the data for the 11 canines studied. To account for differences in the positioning of the individual dog hearts relative to the X-ray beam, a normalized correlation method (Barnea and Silverman, 1972) was used to line up the individual canine data sets based upon overall cardiac shape. Generally only small shifts ( < 4 mm) in the data grids were required. The displacement at each grid intersection at each time point during the cardiac cycle was taken as a simple average of the 11 canines studied. Isovolumic contraction was defined as the time interval between the peak of the R-wave and the opening of the aortic valve. Aortic valve opening was assumed to occur at the crossing of the left ventricular (LV) and aortic (AO) pressure waves. The ejection period was taken as the time between the opening and closing of the aortic valve. Diastole was defined as the time interval from the end of ejection to the peak of the R-wave. The end of ejection was determined from the dicrotic notch on aortic pressure tracings. Isovolumic relaxation was taken as the time period between closing of the aortic valve (dicrotic notch) to opening of the mitral valve. Opening of the mitral valve was assumed to occur when LV pressure fell to 5 mmHg above end-diastolic pressure (EDP). Ventriculogram tracings were used to identify and outline the approximate location of the ventricular chambers, aorta, and pulmonary artery relative to the epicardial data waveform grids. Left and right epicardial surface maps show-

Y

x

X-Ray Beam Axii

(A) Heart

Left Heatt

(8) Data Acquisition Grid

Fig.2. Orientationof the canineheartsduringdata acquisition.Displacements and velocitiesof the epicardial surfaces aremeasured at thegridintersections shownin PanelBalongadirectionparallelto the X axis.The gridshownin B wasconstructed fromdetectorpositioning datafroma caninestudy.

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J. J. McInemeyet al.

ing the magnitudeand timing of systolic velocitiesand displacementsfor an averagenormal canine were created. Timingsin thesemapsare referencedto the peak of the R-wave.Analogousveiocity and displacementmaps were created for the diastolic time interval. Regional inward (toward the septum)and outward displacements and velocitieswere calculatedfor the basicsegmentsof the cardiac cycle. A measureof the variability betweencanineswasobtained by calculating averagedisplacementsof the left ventricular surfaceduring isovolumiccontraction, ejection and isovolumicrelaxation for eachcanine.The left ventricular surfacefor thesecalculationswasdefinedas thosepixelsbetweenthe tip of the apex and the baseof the LV cavity.

RESULTS

For both left and right epicardial surfacesregional motion patterns vary smoothly from region to region (Figs 3 and 4). Surfacedisplacements on both sidesof the heartare largestover regionscoveringthe left ventricular chamberand becomequite smallin areasjust basalto the LV chamber outline. Larger displacementwaveforms reappearat the very baseend of the heart beyond the LV chamberin the region of the large vessels(Fig. 3, Region Bf.

RegionA

During the isovolumiccontraction period,the portion of the left epicardial surfacecovering the LV chamber undergoesa high velocity outward displacementas the heart assumes a moresphericalshape(Figs 3 and 5).This outward bulging is manifestedby the rapid signal increaseshown in the displacementwaveforms during isovolumic contraction (Fig. 3) and by the hot colors (yellow-reds)on the color velocity map (Fig. 5) during frames2-6. This outward expansionreachesits maximumdisplacement just prior to the openingof the aortic valve (frame 9). Left sidesurfacevelocities were larger during isovolumic contraction than at any other time during the cardiac cycle, reaching 64 mms-’ (cf. Table 1). During later isovolumic contraction and very early ejection (frames7-10) there is a smalleroutward movementalong the posterior basaledgeof the heart in the vicinity of the large vesselsand left atrium. This is most easilyseenby a darkeningof the hot colorson the lower right portion of frames7-9 in the LV velocity color plot (Fig. 5). In later isovolumiccontraction there is also an inward motion nearthe tip of the apex(Fig. 5, frames 5-8). Ejection(Fig. 5 frame7, andFig. 7) ismarkedon the left epicardialsurfaceby an inward velocity initiating along the posterioredgeof the heart that spreadsacrossthe base to mergewith a smallerinward velocity wavefront initiated at the anterior base(frames9 and 10).The inward velocity pattern then proceedstoward the apexand basal

LV Chamber / RV Chamber

Fig. 3. Displacement waveforms at theleft lateralepicardial interface.Eachwaveformshowsthedisplacementpatternfor onecardiaccycle.Transitions in displacement waveformshape. acegradualfromregionto region.(A) Approximateregionof the left lateralfreewalladjacentto theLV chamber, (B) regionof the largevessels, (C)posteriorwallwaveformshowing little netinwardmotionduringisovoluukcontraction, (D)waveformshowing transientoutwarddisplacement in theareaof theleftatrium at the start ejection,(E) region nearthebaseof the LV chamber showinga small local outward displacement at the approximate time of aortic valve closure.

Epicardial surface dynamics

1323 lscvolumic elaxation

lSOVUklllliC

Region A

Conlraotion

RV Chamber

Djwywz”

Pr9SSU~ Adic

E-n UJYI I I I bII

I I II I

CL II

II I

II

I

LV Chamber Fig. 4. Displacement waveforms at the right lateral epicardial interface. Each waveform shows the displacement pattern for one cardiac cycle. Displacement patterns are strikingly more uniform than those of the left heart. (A) Approximate region of the right lateral free wall contiguous to the LV and RV chambers, (B) region along the approximate path of the pulmonary artery showing an outward expansion during ejection.

Table 1. Epicardial displacements and velocities during the cardiac cycle Frames

l-6 Isovol contract

Period

7-21 Ejection

22-30

31-34

35-50

Isovol relax

Rapid refill

Later diastole

L.eji side A

Peak velocity (mm s- i) Average peak velocity (mm s- ‘) Peak displacement (mm) Average displacement (mm) Right

64

- 39

37.9 f 14.6 2.6

(S.D.) - 15.1 + 7.9

1.6 k 0.6

- 1.2 f 0.7

53 28.4 + 12.2

-23 - 15.5 & 3.9 - 1.7 - 1.2 + 0.3

- 3.2

- 39 - 2.1 - 0.9 f 0.6

- 16 - 8.7 If: 4.6 - 0.6 - 0.3 If: 0.2

20 10.8 + 3.5 1.8 0.9 + 0.3

-26 - 13 k 6.2 - 1.9 - 0.9 f 0.5

-20 - 7.7 + 5.3 - 0.8 - 0.2 * 0.2

13 9.1 & 2.4

- 17.6 + 8.1

side A

Peak velocity (mm s- ‘) Average peak velocity (mm s- ‘) Peak displacement (mm) Average displacement (mm)

2.1 11.2 + 0.5

1.1 0.6 k 0.2

Average and peak surface displacements and velocities in the normal canine heart during cardiac cycle. Results are based upon an average of the displacement data at each grid location and time point during the cardiac cycle for the 11 canines studied. Positive displacements and velocities are toward the chest wall while negative displacements are toward the septum. Region A on both sides of the heart covers an area contiguous to the left venticular chamber as seen from a left lateral view (see Figs 3 and 4). S.D. = standard deviation.

structures. During frames9-12 (earliestejection)the velocity of the tip of the apex reversesfrom its inward

isovolumiccontraction. The converseis true for the posterior displacements. The averageLV inward displacedirection during isovolumic contraction to an outward ment during ejection in Region A (Fig. 3) was direction. The LV inward displacements during ejection 1.2f 0.7mm (S.D.),with a peakdisplacementand veloare greatestalong the posterior and basalfree wall and city of 3.2 mm and 39mms-l, respectively (Table 1). diminishuniformly in the anterior and apical directions Overall, the regionimmediatelycontiguousto the baseof (Figs3 and 8). In general,displacementsof the anterior the LV chamber (to the right of Region A in (Fig. 3) wall during ejection are substantially smallerthan the showslittle motion during the cardiac cycle. There is, outward expansionsthat occurin the sameregionduring however, a small (OS-l.0 mm) outward displacement

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J. J. Mdnemey

there that peaks at the end of isovolumic contraction and the start of ejection (Fig. 3D, and Fig. 5 frames 8-10). In the anterior region of the large vessels (Region B) there is an inward displacement (0.2-1.9 mm) averaging 1.2 f 0.5 mm (S.D.) during early ejection. The time difference between the onset of a frank inward velocity during ejection at the posterior base of the heart (frame 7) relative to that at the tip of the apex is 80-90 ms (Figs 5 and 7A). Ejection displacements and velocities near the posterior base of the heart during systole are 46 times greater than those of the anterior and apex (Figs 8A and 9A). End-systole (aortic valve closure) occurs at approximately frame 21 (Fig. 5) and is marked by a brief period (approximately 40 ms, frames 21-23) with minimal inward ventricular movement and is followed during isovolumic relaxation and early rapid inflow (frames 24-34) with a mid-anterior inward wall displacement with velocities 2-3 times greater than those in the same area during ejection (Figs 5,lOA and 11A). This midanterior inward motion is accompanied by a brief outward bulging near the apex (frames 23-27, Fig. 5). The average inward wall displacement, over the Region A in Fig. 3, was 0.9 + 0.6 mm (S.D.) during isovolumic relaxation and 0.3 + 0.2 mm (S.D.) during rapid refill, with peak inward displacements of 2.1 mm and 0.6 mm, respectively (Table 1). As this inward displacement over the LV chamber deepens and spreads toward the apex, the anterior basal regions near the large vessels (Region B, Fig. 3) show a persistent outward velocity (frames 25-30, Fig. 5). Maximum inward velocities during early diastole are greatest over the more central or anterior portions of the LV chamber (Fig. 11A). Inward displacements covering the anterior half of the LV chamber during early diastole (Fig. 10) exceed those for the same region during ejection (Fig. 8), while the converse is true for the posterior portions of the ventricle. Maximum diastolic inward velocities occur 80-130 ms after closing of the aortic valve. During the remainder of the cardiac cycle, the LV epicardial surface moves toward the lateral chest wall as the heart fills for the next beat. Right ventricular displacement waveforms (Fig. 4) are fairly uniform in character and do not show the rich regional variation seen on the LV. The apical and more posterior portions of the right ventricle lie contiguous to the mid-anterior portion of the LV chamber. As with the LV, the right ventricular surface also bulges outward during isovolumic contraction (Fig. 6, frames 3-8). Outward bulging is most pronounced toward the distal end of the RV chamber in the region where the LV and RV chambers overlap in the lateral projection. Isovolumic bulging on the right heart is delayed relative to the left by approximately 1 frame (13 ms). Outward expansion reaches its maximum at the approximate time of opening of the aortic valve with a peak displacement and velocity of 2.1 mm and 53 mms-‘, respectively (cf. Table 1). Displacements of the RV contiguous to its outiow tract (Fig. 4) and in the region of the pulmonary artery are small during isovolumic contraction as well as during the remainder of the cardiac cycle. There is no significant

et al.

outward bulge during isovolumic contraction in this area. Ejection on the right side is marked by an inward velocity that initiates along the posterior base of the heart (frame 6, Fig. 6) and then spreads toward the apex, following a path generally along the long axis of the heart. During later systole there is.a brief outward expansion along the path of the pulmonary artery (frames 12~14, Figs 4 and 6). The peak inward displacement and velocity on the right heart during ejection were 1.7 mm and 23 mm s-l, respectively. Maximum inward displacements and velocities during ejection on the right side tended to occur over the region of the RV chamber contiguous to the left ventricle while those on the lower portions of the ventricle were up to 50% smaller (Figs 8B and 9B). These patterns are opposite to those observed for the LV. The hesitation between the inward motion of ejection and the inward motion during isovolumic relaxation observed on the left epicardial surface (frames 21-23, Fig. 5) did not manifest on the RV. For the latter the inward motion from ejection to relaxation was continuous from frames 22 to 34 with maximum inward velocities increasing only slightly during isovolumic relaxation (Figs 9B and 11B). The peak right side inward displacement and velocity (Region A, Fig. 4) during isovolumic relaxation were 1.9 mm and 26 mm s-l, respectively (cf. Table 1) with larger displacements and velocities occurring over the distal portion of the RV chamber outline (Figs 10B and 11B). The distal inward displacements on the RV during isovolumic relaxation and early rapid refill are larger than those for the same region during systole. As on the left side, the right epicardial surface expands outward toward the chest wall during later diastole as the heart chamber refills (frames 35-50). Individual canine displacements for isovolumic contraction, ejection, and isovolumic relaxation for the left ventricular surface averaged 1.4 + 0.6 mm (S.D.), 1.2 + 0.5 mm (S.D.), and 0.8 f 0.4 mm (S.D.) respectively.

DISCUSSION

Past studies of epicardial surface dynamics have been restricted to monitoring projected silhouettes or tracking relatively few specific points on the heart. The latter studies often require surgical procedures to attach markers to myocardium. These procedures, unfortunately, disturb the motion patterns one is trying to measure. The Compton backscatter measurement technique used in this paper does not require surgical or other procedures that could alter the measured data, and permits measurement at many locations of the epicardial interface at many time points during the cardiac cycle. There are some limitations associated with the Compton backscatter imaging (CBI) technique. Like ventriculography and most other currently used medical imaging modalities, the X-ray scatter technique does not track specific material points but rather monitors overall shape. That is, if the epicardial interface is displaced at an angle relative to the incident X-ray beam, the distance

Fig. 5. Color coded velocity map of the left lateral free wall for the complete cardiac cycle. Negative velocities (cool colors) indicate motion away from the chest wall. The orientation of the heart is as shown in Fig. 3. Frames are at 13.3 ms intervals. The EKG shows the timing of the cardiac cycle at the end of each row. Frames 7-24 show the evolution of the inward velocity wave during ejection. Frames 25-34 show a second inward velocity component occurring during early diastole. ED-enddiastole; AVO--aortic valve opening; ES--end-systole; MVO-mitral valve opening.

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Fig. 6. Color coded velocity map of the right lateral free wall for the complete cardiac cycle. Negative velocities (cool colors) indicate motion away from the cheat wall. The orientation of the heart is as shown in Fig. 4. Frames are at 13.3 ms intervals. The EKG shows the timing of the cardiac cycle at the end of each row. Frames 7-24 show the evolution of the inward velocity wave during ejection. Frames 25-34 show a second inward velocity component occurring during early diastole. Unlike the left heart, inward diastolic velocities are more continuous with those of systole. ED--end-diastole; AVG-aortic valve opening; ES--end-systole; MVO-mitral valve opening.

1326

Epicardial surface dynamics

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6. :

(A) Left Surface

(B) Right Surface

Timing of Initial InwardWall Motion During Ejection(msec) Fig. 7. Timing of initial inward wall motion during ejection. Times are in milliseconds relative to the peak of the R-wave. On the left heart inward motion during systole occurs 680 ms earlier near the posterior base than at the apex. Similar results are shown in Panel B for the right heart except that the earliest inward motion occurs over the region contiguous to the LV and RV outflow tracts.

(A) Left Surface

(B) Right Surface

Inward DisplacementsDuringEjection (mm) Fig. 8. Regional left and right heart peak lateral wall inward displacements (mm) during ejection. On the left heart, posterior inward displacement during ejection is approximately 3-8 times larger than that at the anterior. Displacements on the right heart tend to be more uniformly distributed across the areas of the ventricles. For’both the left and right sides, displacements during ejection tend to be smaller over regions contiguous to the LV and RV outflow tracts.

traveled by the interface along the beam path will be greater than the displacementof a specific landmark perpendicularto the surface.Nevertheless,splinefitting the coordinatesof the acquiredX-ray scatterdata setstill will accurately describethe three-dimensionalshapeof the heart during the cardiac cycle since the shapeis definedby any data set along the boundary. The X-ray scattertechniquewill alsonot detectpurerotations of the heart, unlesssuch rotations produce tissueexcursions

alongthe path of the incomingX-ray beam.Rotationsof the lateral free walls are relatively small,generally less than 10” (Hansenet al., 1988),and result in tangential translationswith most tissueat any location remaining within the samebackscatterdetector’ssensitivevolume. Rotations will consequentlyhave only minor effectson the general character of the resultswe have reported. Partial volumeeffectswill give incorrect surfacedisplacementswhen a detector sensitivevolume only partially

J. J. McInerney et al.

1328

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Peak Lateral Wall Ejection Velocities (mmkec) Fig.9. Regional left andrightheartpeaklateralwallinwardvelocities (mm-’ s)duringejection. On theleft sidepeakinwardvelocitiesnearthe posteriorbaseof the heartare24 timeslargerthan thoseon the anterior.Peak velocities on the right heart tend to be more uniformly distributed.

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(A) Left Surface

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Lateral Wall Inward Displacements During Early Diastde (mm) Fig. 10. Regional left and right heart lateral wall inward displacements (mm) during isovolumic relaxation and early rapid refill. The magnitudes of displacements duriq diastole are approximately the same as those that occurred during systole. Peak displacement onbothsidesof theheartoccurs on themid-lateralwalls.

tills with cardiac tissueduring its initial outward scan. Theseeffectswereexcludedin thesestudiesby not including data from the anterior or posterior boundaries.The measurement techniqueis also limited to the epicardial free walls. The dominant conformationchangeon the LV lateral wall during isovolumic contraction is the change to a moresphericalshapeasthe lateral wall bulgesoutward whilethe apex,baseend and the posteriorportion of the wall in later isovohnniccontraction aredisplacedinward. Theseresultsare consistentwith thosein instrumented closed-cheststudies(Hinds et al., 1969;Rushmeret al.,

1953)and in dogswith open chestor reducedend-diastolic volumes(Rankin et al., 1976-open chest),but are in disagreementwith those of others (Bove, 1971; McDonald, 1970;Rankin et al., 1976-closed chest)who showdecreaseddiametersduring this sametime period. The studiesof McDonald (1970)and Rankin et al. (1976) were both performed on surgically instrumenteddogs raising the possibility of motion abnormalitiesimposed by post-surgicaladhesions.A more lik@ explanation is the limited surfacecoverageof transd&oerand marker placementswhich in thesestudieswere&r an A-P plane approximately parallelto the septumand perpendicular

Epicardial surface dynamics

(A) Left Surface

1329

(B) Right Surface

Peak Lateral Wall Inward Velocities During Early Diastole (mm/se@ Fig. 11. Regional left and right heart peak lateral wall inward velocities (mm-l s) during isovolumic relaxation and early rapid refill. The magnitudes of peak velocitiesduring d&stole are approximately the same as those that occurred during systole. Peak velocities for both sides of the heart occur on the mid-lateral wall near the apex.

to our measurement direction. This is consistent with the small net displacement change we observe during isovolumic contraction at the extreme anterior or posterior measurement sites. At the most anterior sites (Fig. 3) the displacements during isovolumic contraction are small while those at the most posterior positions show an inward movement after an initial outward bulging (Fig. 3C). These effects combined with wall thickening during isovolumic contraction could very well lead to the net reduction of measured internal diameters during isovolumic contraction. The inward motion noted in the displacement waveforms at the posterior base of the heart during later isovolumic contraction is also consistent with the contraction of the inflow tract at that time noted by other authors (Bove, 1971; Hinds et al., 1969). Motion patterns on the RV epicardial surface show considerably less variation than those on the LV. The primary event for the RV free wall during isovolumic contraction is an outward expansion that is consistent with findings of March et al. (1962) and Raines et al. (1976). The primary feature on the left side epicardial surface during ejection is the inward velocity wave that initiates (frames 7 and 8, Fig. 5) in the area of the inflow tract and spreads across the base and then towards a relatively fixed apex. During the early ejection frames the tip of the apex was noted to have an outward directed velocity (cf. Fig. 5, frames 9-12). This early systolic outward motion could result from the inability of the thinner myocardium at the apex to overcome early pressure increases as the vigorous contraction of the posterior heart near the inflow tract drives blood in an apical and anterior direction. The overall pattern of early ejection velocities is consistent with electrical studies (Durrer et al., 1970;

Klausner et al., 1982) that show two of the three earliest depolarization sites occurring high on the paraseptal wall and at the posterior paraseptal area about one-third of the distance from the apex to the base. In our studies the inward velocity wavefronts from these general areas converge at approximately 20-30 ms (frames 9 and 10, Fig. 5) after their first manifestation. This is in agreement with the corresponding electrical measurements of Durrer et al. (1970). The latter author finds activation proceeding next toward the apex and lastly toward the posterior basal area We find the apex and posterior basal areas begin their inward movement more or less simultaneously probably due to simple mechanical tethering. Our results do not agree with the findings of Kong et al. (1971) who report that mechanical activation begins first at the anterior septal area at the apex before proceeding toward the base and posterior. The findings of Kong et al., however, were determined from epicardial segment length changes between bifurcations of the coronary arteries or attached metal markers. Epicardial fibers in general are obliquely longitudinal (Streeter et al., 1969) and consequently move in directions perpendicular to our displacement measurements. As such, the results of Kong et al. are not necessarily inconsistent with our data. Also, Durrer et al. (1970) found left epicardial activation quite variable and did document in some cases where there was activation of the apex before the base. Our findings that displacements and velocities during ejection are larger toward the base and posterior regions of the LV are consistent with many others (Haendchen et al., 1983; Ingels et al., 1981; Potel et a/., 1983; Slager et al., 1986). Ingels et al. (1990) used metal markers in transplanted hearts to demonstrate that the heart pumped with a double bellows action with the free walls displacing

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inward toward a relatively immobile septum. Our results, with largest inward displacement during ejection occurring along the posterior, suggest that the bellows action may be pivoted toward the anterior heart. Such an action is teleologically pleasing in that it would tend to appose the papillary muscles and direct blood from the inflow to the outflow tract. The finding that inward motion of the base precedes that of the apex is in agreement with the results of Hinds et al. (1969) and Hammermeister et al. (1986) and confirms the latter’s hypothesis that the reported delay in mechanical activation between the apex and base is not an artifact but a real entity. The studies reported in this paper were performed with breath held in end-inspiration. Earlier studies (McInerney et al., 1984, 1989) with breath held in end-expiration show a strong inward displacement during atria1 contraction in the region proximal to the base of the LV chamber, identifying this area as left atrium. The small bump on the waveforms in this vicinity (Fig. 3D) peaking at the start of ejection is probably due to a displacement of the mitral valve into the LA during contraction. The larger inward displacements in the vicinity of and to the right of the outline of the pulmonary artery (Fig. 3, Region B) are somewhat of a mystery. Similar waveforms, but of considerably smaller magnitude and earlier in the contraction cycle, also appear on the right side of the heart near the pulmonary artery and RV outflow tract. Our inclination was to expect an outward displacement in this region as the aorta expanded during early ejection. One possibility could be an inward motion of the region of the pulmonary artery due to the tethering of the latter to the aorta via the fibrotic ductus arteriosis. As the aorta expands during ejection the arch would have a tendency to straighten and pull on the pulmonary artery. On the RV epicardial surface the region of the RV outflow tract remained essentially stationary during the cardiac cycle. The absence in this region of an outward expansion during isovolumic contraction and the brief outward expansion along the path of the pulmonary artery during systole (Fig. 4B) are in agreement with the findings of others (March et al., 1962;Raineset al., 1976). We did not find evidenceof an obvious peristalticaction in the RV directedtoward the outflow tract assuggested by Raineset al. (1976). Early diastole is marked by an unexpectedinward motion on the mid-lateraland anterior free wallsof both ventricles that is initiated during isovolumic relaxation shortly after maximum negative LV dp/dt (Mclnemey et al., 1989).There is a tendency for the posterolateral wall to expand outward in the sametime period. Most authors report expansivemovementsin the LV during isovolumicrelaxation and rapid refill, including outward displacementof the lateral walls,suddenincreases in base to apex length, or ballooning out in apical areasof the heart prior to cross-sectionalexpansion(Altieri et al., 1973;Bove, 1971;Brower et al., 1977;Gibsonet al., 1976; Hammermeisteret al., 1986).Our resultsdo confirm an outward expansionin the area of the LV apex during early isovolumicrelaxation (frames23-27,Fig. 5)but not the early global outward movementof the LV or RV free

walls. One possibleexplanation for this discrepancy could be the effect of wall thinning. Rankin et al. (1976), for example,reported that the anterior LV wall thinned during isovolumic relaxation in every dog in his study. This effect would reconcilethe inward motion we see with the outward motion reported by the others.Nevertheless,elementalconservationprinciplesrequireinward motion somewherein the LV during isovolumicrelaxation if other areas are expanding outward. Some authors have indeed reported transient inward movementsduring this time period.Grover and Glantz (1983), usingradiopaquemarkers,frequently observedtransient inward wall movementsof the lateral LV free wall close to the time of LV (dp/dt) minimum.Similarly, Brower et al. (1977) noted in canine studies a reduction in LV chamber diameter during the sametime period. The latter author noted some LV diametersup to 2 mm smallerduring the relaxation period than they were at end ejection.An inward motion of the anterior endocardial walls during isovolumic relaxation could easily be missedin the 30” RAO view used in most ventriculograpic-basedstudies since the LV border projected is usuallythat of the largestchamberdimensions. There are alsothe usualproblemswith the contrast-basedboundary definitions(Hallermanet al., 1963;Ingelset al., 1980; Slageret al., 1986).One possibleforceto createaninward movement during early diastole is diastolic suction. A rapid pressuredrop, augmentedby the rapid expansionof the LV chamber,hasbeendemonstrated(Brecher, 1956;Hori et al., 1982;Sugaet al., 1986).Nevertheless,for suchan effect to result in an inward displacementof the anterolateral wall, LV cavity pressureswould have to drop to levelslower than those of the thoracic cavity. Another possiblemechanismis the subepicardialtone reportedby Stein et al. (1980,1985)for the anterolateral wall during this time period. A simultaneoustensingof the subepicardialfibers and relaxation of endocardial fibers would tend to causethe wall to flex inward in a manneranalogousto what happensto a bimetallicstrip under a temperaturechange. In the work reportedhere,wehave studiedthe dynamically changingshapeof the heart at many time points during the completecardiaccycle and at severalhundred locationsat the epicardialinterface.For the first time, it was possibleto examinein detail the patterns of shape changefrom regionto regionon the left and right sidesof the heart. Our resultshave co~u%rned and coordinated the findingsof many othersand haveaddednewinformation. We haveshownthat whereasmotion patternsof the right heart tend to be fairly uniform, those on the left show considerablymore regional variability. Although the finding of differencesin regionalmotion patterns of the left heart is not new, our results show that these differencesevolve smoothly from region to region. We have alsodemonstratedan unexpectedinward motion of both sidesof the heart during early diastole.Overall, the regionalepicardialmotion patternsduring early diastole are found to be the oppositeof those occurring during systole.That is,during early systoleinward displacement on the posterior LV is significantly greater than that of

Epicardial surface dynamics

the anterior, while during isovolumic relaxation and rapid refill, the reverseis true. Although inward motion during early diastole could be due to wall thinning, circumstantialevidencesuggests it may be manifestedat the endocardiumalso. If suchis the case,it could have important ramifications for many studiesin the past which have usedthe end of inward motion asthe marker for end-systole. The resultsof this study, or analogousstudieswith ischemicor infarcted hearts, could be usedas surface boundary conditionsfor a biomechanicalmodelof heart deformation and responseto pressureforcing functions. The measurementmethod also has potential as a noninvasive tool for serialstudiesof cardiac motion abnormalities. Acknowledgement-This work was supported by grants from The National Institutes of Health, Heart, Lung, and Blood Institute (PHS 1 ROl-HL40969) and from the Delaware Affiliate of the American Heart Association. REFERENCES

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